The arrival of Tony Mowbray later that year saw Whittaker confirmed in the team's right back role, and with this new certainty, he flourished, becoming a regular in the Scotland Under–21 team and helping Hibernian to a third place league finish. Whittaker was a regular in the Hibs teams of both Mowbray and John Collins, and was in the side that won the 2007 League Cup Final. He made 174 appearances in all competitions for Hibs, scoring five goals.

Whittaker completed a £2m move to Rangers on 1 August 2007, signing a five-year contract.[7] He was given the number 28 shirt and started his first game for Rangers on 18 August 2007 against Falkirk in the Scottish Premier League and marked his debut with the second goal in a 7–2 win for Rangers.[8] Having been deployed mostly at left back during the first half of the season, Whittaker established himself as first-choice right back after Alan Hutton's departure to Tottenham Hotspur in January 2008. Whittaker scored the second goal of Rangers 2–0 win over Sporting Lisbon in the UEFA Cup quarter-final second-leg on 10 April 2008.[9] He picked the ball up on the halfway line and weaved past several players before capping it off with a cool finish. He stated after the match that it was the best goal of his career.[10]

For the 2009–10 season, Whittaker was given number 16 and scored 11 goals in all competitions as Rangers won both the league title and the League Cup.

Whittaker signed a new five-year contract with Rangers in July 2011, after the club had rejected bids from Turkish club Bursaspor.[11] During the UEFA champions league qualifiers against Malmo FF, he was sent off for throwing the ball at an opponent player after receiving a poor tackle.

In June 2012, Whittaker lodged an objection against his contract being transferred from Rangers to a new company set up by Charles Green.[12]PFA Scotland had previously commented that players were entitled to become free agents if they objected to the transfer.[13] Whittaker explained in the news conference, saying "We owe no loyalty to the new club. There is no history there for us."[12]

Whittaker signed for English Premier League club Norwich City on 30 June 2012, signing a four-year deal.[14] Following his move, Whittaker stated that he was happy with a move to Norwich.[15] On 20 July, Whittaker received provisional international clearance from FIFA which allowed him to play while arbitration over his move from Rangers continued.[16]

Whittaker suffered an ankle injury during a friendly match against Celtic,[17] which caused him to miss the start of the 2012–13 Premier League season. Two months after receiving his ankle injury, he described it as the worst of his career.[18] He made his competitive debut for Norwich on 31 October, playing at right back in a 2–1 win against Tottenham Hotspur. A few days later, Whittaker made his league debut for the club, playing at right back and stayed on the pitch for 90 minutes, in a 1–0 win over Stoke City. After making his debut, Whittaker said he was pleased to make his debut with a win.[19] The following month on 8 December 2012, Whittaker scored his first goal in his Premier League career after an assist from Robert Snodgrass in a 4–3 win over Swansea City.[20]

Whittaker scored in the opening game of the 2013-14 Premier League season with a goal against Everton. His blasted shot struck the post and bounced back out, but he beat Tim Howard to the rebound to tap it back in. He also assisted débuting team-mate Ricky van Wolfswinkel; Whittaker sliced a shot with his foot which floated toward van Wolfswinkel, who was free to header it into the goal.[citation needed]

Whittaker was a regular for the Scotland U21 squad, and in October 2006 he was added to the full Scotland squad for the Euro 2008 qualifying match against Ukraine, although he did not feature in the match.[21] Whittaker was then called into the Scotland B side to face Republic of Ireland's B team on 20 November 2007.[22] He played 68 minutes before being replaced by Ross McCormack.[23] He also played in the goalless draw between those two sides in November 2006.[24]